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Common protein sequence signatures associate with Sclerotinia borealis lifestyle and secretion in fungal pathogens of the Sclerotiniaceae.

Badet T, Peyraud R, Raffaele S - Front Plant Sci (2015)

Bottom Line: To spread successfully, S. borealis must synthesize proteins adapted to function in its specific environment.We found that enrichment in Thr, depletion in Glu and Lys, and low disorder frequency in hot loops are significantly associated with S. borealis proteins.High index proteins were also enriched in function associated with plant colonization in S. borealis, and in in planta-induced genes in S. sclerotiorum.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire des Interactions Plantes-Microorganismes, Institut National de la Recherche Agronomique, UMR441 Castanet-Tolosan, France ; Laboratoire des Interactions Plantes-Microorganismes, Centre National de la Recherche Scientifique, UMR2594 Castanet-Tolosan, France.

ABSTRACT
Fungal plant pathogens produce secreted proteins adapted to function outside fungal cells to facilitate colonization of their hosts. In many cases such as for fungi from the Sclerotiniaceae family the repertoire and function of secreted proteins remains elusive. In the Sclerotiniaceae, whereas Sclerotinia sclerotiorum and Botrytis cinerea are cosmopolitan broad host-range plant pathogens, Sclerotinia borealis has a psychrophilic lifestyle with a low optimal growth temperature, a narrow host range and geographic distribution. To spread successfully, S. borealis must synthesize proteins adapted to function in its specific environment. The search for signatures of adaptation to S. borealis lifestyle may therefore help revealing proteins critical for colonization of the environment by Sclerotiniaceae fungi. Here, we analyzed amino acids usage and intrinsic protein disorder in alignments of groups of orthologous proteins from the three Sclerotiniaceae species. We found that enrichment in Thr, depletion in Glu and Lys, and low disorder frequency in hot loops are significantly associated with S. borealis proteins. We designed an index to report bias in these properties and found that high index proteins were enriched among secreted proteins in the three Sclerotiniaceae fungi. High index proteins were also enriched in function associated with plant colonization in S. borealis, and in in planta-induced genes in S. sclerotiorum. We highlight a novel putative antifreeze protein and a novel putative lytic polysaccharide monooxygenase identified through our pipeline as candidate proteins involved in colonization of the environment. Our findings suggest that similar protein signatures associate with S. borealis lifestyle and with secretion in the Sclerotiniaceae. These signatures may be useful for identifying proteins of interest as targets for the management of plant diseases.

No MeSH data available.


Related in: MedlinePlus

Network representation of gene ontologies (GOs) of proteins with sTEKhot >1 in S. borealis proteome. Nodes correspond to GOs are sized according to the number of proteins with sTEKhot >1. They are colored from yellow to orange according to the p-value of a hypergeometric test for enrichment in proteins with sTEKhot >1 compared to whole proteomes. White nodes are GOs not significantly enriched among proteins with sTEKhot > 1 (p>0.05). GOs labeled in bold font correspond to functions possibly associated with host interaction.
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Figure 5: Network representation of gene ontologies (GOs) of proteins with sTEKhot >1 in S. borealis proteome. Nodes correspond to GOs are sized according to the number of proteins with sTEKhot >1. They are colored from yellow to orange according to the p-value of a hypergeometric test for enrichment in proteins with sTEKhot >1 compared to whole proteomes. White nodes are GOs not significantly enriched among proteins with sTEKhot > 1 (p>0.05). GOs labeled in bold font correspond to functions possibly associated with host interaction.

Mentions: To identify protein functions important for adaptation to S. borealis environment, we analyzed annotations of proteins with a sTEKhot value higher than 1 in S. borealis proteome. Overall, 4794 (47%) S. borealis proteins had no Gene Ontology (GO) annotation assigned. There were 635 proteins with sTEKhot > 1, among which 349 (55%) had no GO annotation. We looked for GO term enrichment in the 635 S. borealis with sTEKhot > 1 compared to all annotated proteins. Forty two GO terms appeared significantly enriched (p < 0.05) among proteins with sTEKhot > 1, including 16 leaves (GO with no child term) of the GO network (Figure 5). GO terms for “cellular component” enriched in proteins with sTEKhot > 1 included extracellular and cell wall compartments. Consistently, enriched “biological processes” and “molecular functions” related to secreted enzymes involved in cell wall modification (glycosyl hydrolases and carboxylic ester hydrolases, among which are pectinesterases and cutinases) and binding to cellulose. Cellulose is a major component of plant cell walls that fungal pathogens are able to detect and bind. Also plants aerial parts are protected by a cuticle composed by cutin. Fungal pathogens are able to hydrolyze cutin through cutinases, thus facilitating host colonization. In addition, proteins involved in carbohydrate metabolism were enriched among proteins with sTEKhot > 1. These functions are associated with colonization of the environment, especially plant-associated environment. Similar enrichments where observed when looking at GO annotations for S. sclerotiorum and B. cinerea proteins harboring a sTEKhot > 1 (Figures S1, S2). In addition, copper ion binding GO was found to be enriched in S. sclerotiorum and B. cinerea.


Common protein sequence signatures associate with Sclerotinia borealis lifestyle and secretion in fungal pathogens of the Sclerotiniaceae.

Badet T, Peyraud R, Raffaele S - Front Plant Sci (2015)

Network representation of gene ontologies (GOs) of proteins with sTEKhot >1 in S. borealis proteome. Nodes correspond to GOs are sized according to the number of proteins with sTEKhot >1. They are colored from yellow to orange according to the p-value of a hypergeometric test for enrichment in proteins with sTEKhot >1 compared to whole proteomes. White nodes are GOs not significantly enriched among proteins with sTEKhot > 1 (p>0.05). GOs labeled in bold font correspond to functions possibly associated with host interaction.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4585107&req=5

Figure 5: Network representation of gene ontologies (GOs) of proteins with sTEKhot >1 in S. borealis proteome. Nodes correspond to GOs are sized according to the number of proteins with sTEKhot >1. They are colored from yellow to orange according to the p-value of a hypergeometric test for enrichment in proteins with sTEKhot >1 compared to whole proteomes. White nodes are GOs not significantly enriched among proteins with sTEKhot > 1 (p>0.05). GOs labeled in bold font correspond to functions possibly associated with host interaction.
Mentions: To identify protein functions important for adaptation to S. borealis environment, we analyzed annotations of proteins with a sTEKhot value higher than 1 in S. borealis proteome. Overall, 4794 (47%) S. borealis proteins had no Gene Ontology (GO) annotation assigned. There were 635 proteins with sTEKhot > 1, among which 349 (55%) had no GO annotation. We looked for GO term enrichment in the 635 S. borealis with sTEKhot > 1 compared to all annotated proteins. Forty two GO terms appeared significantly enriched (p < 0.05) among proteins with sTEKhot > 1, including 16 leaves (GO with no child term) of the GO network (Figure 5). GO terms for “cellular component” enriched in proteins with sTEKhot > 1 included extracellular and cell wall compartments. Consistently, enriched “biological processes” and “molecular functions” related to secreted enzymes involved in cell wall modification (glycosyl hydrolases and carboxylic ester hydrolases, among which are pectinesterases and cutinases) and binding to cellulose. Cellulose is a major component of plant cell walls that fungal pathogens are able to detect and bind. Also plants aerial parts are protected by a cuticle composed by cutin. Fungal pathogens are able to hydrolyze cutin through cutinases, thus facilitating host colonization. In addition, proteins involved in carbohydrate metabolism were enriched among proteins with sTEKhot > 1. These functions are associated with colonization of the environment, especially plant-associated environment. Similar enrichments where observed when looking at GO annotations for S. sclerotiorum and B. cinerea proteins harboring a sTEKhot > 1 (Figures S1, S2). In addition, copper ion binding GO was found to be enriched in S. sclerotiorum and B. cinerea.

Bottom Line: To spread successfully, S. borealis must synthesize proteins adapted to function in its specific environment.We found that enrichment in Thr, depletion in Glu and Lys, and low disorder frequency in hot loops are significantly associated with S. borealis proteins.High index proteins were also enriched in function associated with plant colonization in S. borealis, and in in planta-induced genes in S. sclerotiorum.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire des Interactions Plantes-Microorganismes, Institut National de la Recherche Agronomique, UMR441 Castanet-Tolosan, France ; Laboratoire des Interactions Plantes-Microorganismes, Centre National de la Recherche Scientifique, UMR2594 Castanet-Tolosan, France.

ABSTRACT
Fungal plant pathogens produce secreted proteins adapted to function outside fungal cells to facilitate colonization of their hosts. In many cases such as for fungi from the Sclerotiniaceae family the repertoire and function of secreted proteins remains elusive. In the Sclerotiniaceae, whereas Sclerotinia sclerotiorum and Botrytis cinerea are cosmopolitan broad host-range plant pathogens, Sclerotinia borealis has a psychrophilic lifestyle with a low optimal growth temperature, a narrow host range and geographic distribution. To spread successfully, S. borealis must synthesize proteins adapted to function in its specific environment. The search for signatures of adaptation to S. borealis lifestyle may therefore help revealing proteins critical for colonization of the environment by Sclerotiniaceae fungi. Here, we analyzed amino acids usage and intrinsic protein disorder in alignments of groups of orthologous proteins from the three Sclerotiniaceae species. We found that enrichment in Thr, depletion in Glu and Lys, and low disorder frequency in hot loops are significantly associated with S. borealis proteins. We designed an index to report bias in these properties and found that high index proteins were enriched among secreted proteins in the three Sclerotiniaceae fungi. High index proteins were also enriched in function associated with plant colonization in S. borealis, and in in planta-induced genes in S. sclerotiorum. We highlight a novel putative antifreeze protein and a novel putative lytic polysaccharide monooxygenase identified through our pipeline as candidate proteins involved in colonization of the environment. Our findings suggest that similar protein signatures associate with S. borealis lifestyle and with secretion in the Sclerotiniaceae. These signatures may be useful for identifying proteins of interest as targets for the management of plant diseases.

No MeSH data available.


Related in: MedlinePlus